Neural correlates of spatial frequency processing: A neuropsychological approach

We examined the neural correlates of spatial frequency (SF) processing through a gender and neuropsychological approach, using a recognition task of filtered (either in low spatial frequencies/LSF or high spatial frequencies/HSF) natural scene images. Experiment 1 provides evidence for hemispheric specialization in SF processing in men (the right hemisphere is predominantly involved in LSF analysis and the left in HSF analysis) but not in women. Experiment 2 aims to investigate the role of the right occipito-temporal cortex in LSF processing with a neurological female patient who had a focal lesion of this region due to an embolization of an arterioveinous malformation. This study was conducted 1 week before and 6 months after the surgical intervention. As expected, after the embolization, LSF scene recognition was more impaired than HSF scene recognition. These data support the hypothesis that the right occipito-temporal cortex might be preferentially specialized for LSF information processing and more generally suggest a hemispheric specialization in SF processing in females, although it is difficult to demonstrate in healthy women.

[1]  F. Kitterle,et al.  Visual field effects in the discrimination of sine-wave gratings , 1991, Perception & psychophysics.

[2]  Bruce E. Wexler,et al.  Changes in perceptual asymmetry with the menstrual cycle , 1989, Neuropsychologia.

[3]  A. Nowicka,et al.  Visual-spatial-frequency model of cerebral asymmetry: a critical survey of behavioral and electrophysiological studies. , 1996, Psychological bulletin.

[4]  O. Güntürkün,et al.  Steroid fluctuations modify functional cerebral asymmetries: the hypothesis of progesterone-mediated interhemispheric decoupling , 2000, Neuropsychologia.

[5]  O. Güntürkün,et al.  Sex Differences in Functional Cerebral Asymmetries in a Repeated Measures Design , 1999, Brain and Cognition.

[6]  Ursula Gather,et al.  Functional cerebral asymmetries during the menstrual cycle: a cross-sectional and longitudinal analysis , 2002, Neuropsychologia.

[7]  E. Zaidel,et al.  Individual differences in lateralization: effects of gender and handedness. , 1997, Neuropsychology.

[8]  D. Tucker.  Sex differences in hemispheric specialization for synthetic visuospatial functions , 1976, Neuropsychologia.

[9]  Shingo Yamagata,et al.  Cerebral Asymmetry of the “Top-Down” Allocation of Attention to Global and Local Features , 2000, The Journal of Neuroscience.

[10]  Stephen Christman,et al.  Visual hemispheric asymmetries depend on which spatial frequencies are task relevant , 1992, Brain and Cognition.

[11]  Ronald Hübner,et al.  The effect of spatial frequency on global precedence and hemispheric differences , 1997, Perception & psychophysics.

[12]  H. Hughes,et al.  Global Precedence, Spatial Frequency Channels, and the Statistics of Natural Images , 1996, Journal of Cognitive Neuroscience.

[13]  L. A. Flashman,et al.  Sex differences in semantic language processing: A functional MRI study , 2003, Brain and Language.

[14]  A. Nowicka,et al.  VISUAL-SPATIAL-FREQUENCY MODEL OF CEREBRAL ASYMMETRY : A CRITICAL SURVEY OF BEHAVIORAL AND ELECTROPHYSIOLOGICAL STUDIES , 1996 .

[15]  J. Hellige,et al.  Individual variation in hemispheric asymmetry: multitask study of effects related to handedness and sex. , 1994, Journal of experimental psychology. General.

[16]  Maryanne Martin,et al.  Hemispheric specialization for local and global processing , 1979, Neuropsychologia.

[17]  L. Katz,et al.  Cerebral organization of component processes in reading. , 1996, Brain : a journal of neurology.

[18]  J. Mcglone,et al.  Sex differences in the cerebral organization of verbal functions in patients with unilateral brain lesions. , 1977, Brain : a journal of neurology.

[19]  D. Navon.  Forest before trees: The precedence of global features in visual perception , 1977, Cognitive Psychology.

[20]  R. Holloway,,et al.  Sexual dimorphism in the human corpus callosum: an extension and replication study. , 1986, Human neurobiology.

[21]  Individual variation in hemispheric asymmetry: multitask study of effects related to handedness and sex. , 1994, Journal of experimental psychology. General.

[22]  Edward T. Bullmore,et al.  Sex Differences in Functional Brain Activation during a Lexical Visual Field Task , 2002, Brain and Language.

[23]  M. Corballis,et al.  Effects of concurrent memory load on visual-field differences in mental rotation , 1993, Neuropsychologia.

[24]  Theodor Landis,et al.  Shift of functional cerebral asymmetry during the menstrual cycle , 1989, Neuropsychologia.

[25]  G. Yovel,et al.  Hemispheric asymmetries for global and local visual perception: effects of stimulus and task factors. , 2001 .

[26]  G L Shulman,et al.  The Role of Spatial-Frequency Channels in the Perception of Local and Global Structure , 1986, Perception.

[27]  M. V. Kleeck.  Hemispheric differences in global versus local processing of hierarchical visual stimuli by normal subjects: New data and a meta-analysis of previous studies , 1989, Neuropsychologia.

[28]  Joseph B. Hellige,et al.  Hemispheric differences are found in the identification, but not the detection, of low versus high spatial frequencies , 1990, Perception & psychophysics.

[29]  Gaspare Galati,et al.  The Contribution of Functional Neuroimaging to Recovery After Brain Damage: A Review , 2001, Cortex.

[30]  Richard S. J. Frackowiak,et al.  Where in the brain does visual attention select the forest and the trees? , 1996, Nature.

[31]  L O Harvey,et al.  Spatial frequencies and the cerebral hemispheres: Contrast sensitivity, visible persistence, and letter classification , 1989, Perception & psychophysics.

[32]  J. Mcglone,et al.  Sex differences in human brain asymmetry: a critical survey , 1980, Behavioral and Brain Sciences.

[33]  Tetsuya Iidaka,et al.  Spatial frequency of visual image modulates neural responses in the temporo-occipital lobe. An investigation with event-related fMRI. , 2004, Brain research. Cognitive brain research.

[34]  H. Rusinek,et al.  Functional magnetic resonance imaging of human brain activity in a verbal fluency task , 1998, Journal of neurology, neurosurgery, and psychiatry.

[35]  D. Voyer,et al.  On the magnitude of laterality effects and sex differences in functional lateralities. , 1996, Laterality.

[36]  M. Buchsbaum,et al.  Hemispheric asymmetry for selective attention. , 2000, Brain research. Cognitive brain research.

[37]  R. Holloway,,et al.  Sexual dimorphism in the human corpus callosum. , 1982, Science.

[38]  S. Kitazawa,et al.  Sex differences in lateralization revealed in the posterior language areas. , 2000, Cerebral cortex.

[39]  L. Robertson,et al.  Neuropsychological contributions to theories of part/whole organization , 1991, Cognitive Psychology.

[40]  G. Mangun,et al.  Neural Mechanisms of Global and Local Processing: A Combined PET and ERP Study , 1998, Journal of Cognitive Neuroscience.

[41]  Antígona Martínez,et al.  Hemispneric asymmetries in global and local processing: evidence from fMRI , 1997, Neuroreport.

[42]  G. Rizzolatti,et al.  Hemispheric Superiority in Reaction Time to Faces: A Sex Difference , 1977, Cortex.

[43]  J. Mcglone,et al.  Sex differences in cerebral processing of visuospatial tasks. , 1973, Cortex; a journal devoted to the study of the nervous system and behavior.

[44]  L. Katz,et al.  Sex differences in the functional organization of the brain for language , 1995, Nature.

[45]  A Zani,et al.  Electrophysiological evidence of a perceptual precedence of global vs. local visual information. , 1998, Brain research. Cognitive brain research.

[46]  Onur Güntürkün,et al.  Sex hormones affect spatial abilities during the menstrual cycle. , 2000 .

[47]  B. Milner,et al.  Right temporal-lobe contribution to global visual processing , 1991, Neuropsychologia.

[48]  R. Knight,et al.  Component mechanisms underlying the processing of hierarchically organized patterns: inferences from patients with unilateral cortical lesions. , 1990, Journal of experimental psychology. Learning, memory, and cognition.

[49]  D. Delis,et al.  Hemispheric specialization of memory for visual hierarchical stimuli , 1986, Neuropsychologia.

[50]  C. Chiarello,et al.  Visual cerebral lateralization over phases of the menstrual cycle: A preliminary investigation , 1989, Brain and Cognition.

[51]  Donna M. Piazza.  The influence of sex and handedness in the hemispheric specialization of verbal and nonverbal tasks , 1980, Neuropsychologia.

[52]  J. Marshall,et al.  Hemispheric asymmetries in global⧹local processing are modulated by perceptual salience , 1998, Neuropsychologia.

[53]  J. Inglis,et al.  Sex Differences in the Cognitive Effects of Unilateral Brain Damage , 1982, Cortex.

[54]  G. R Mangun,et al.  On the processing of spatial frequencies as revealed by evoked-potential source modeling , 2000, Clinical Neurophysiology.

[55]  D. Boles.  Sex in lateralized tachistoscopic word recognition , 1984, Brain and Language.

[56]  Carole Peyrin,et al.  Hemispheric specialization for spatial frequency processing in the analysis of natural scenes , 2003, Brain and Cognition.

[57]  K Zilles,et al.  A functional magnetic resonance imaging study of local/global processing with stimulus presentation in the peripheral visual hemifields , 2004, Neuroscience.

[58]  M. J. Blanca,et al.  Hemispheric differences in global and local processing dependent on exposure duration , 1994, Neuropsychologia.

[59]  L. Robertson,et al.  Effects of lesions of temporal-parietal junction on perceptual and attentional processing in humans , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[60]  R. Gorski,et al.  Sex differences in the corpus callosum of the living human being , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[61]  R. C. Oldfield.  The assessment and analysis of handedness: the Edinburgh inventory. , 1971, Neuropsychologia.

[62]  Lynn C. Robertson,et al.  The neurology of visual attention. , 1995 .

[63]  P. Cormier,et al.  Instruction Effects on Gender Differences in Visual Field Advantages During Lexical Decision Tasks , 1991, Cortex.

[64]  Monica Baciu,et al.  Cerebral regions and hemispheric specialization for processing spatial frequencies during natural scene recognition. An event-related fMRI study , 2004, NeuroImage.

[65]  D R Badcock,et al.  Low-Frequency Filtering and the Processing of Local—Global Stimuli , 1990, Perception.

[66]  S K Mannan,et al.  Scanning the visual world: a study of patients with homonymous hemianopia , 2000, Journal of neurology, neurosurgery, and psychiatry.

[67]  E W Yund,et al.  The role of spatial frequency in the processing of hierarchically organized stimuli , 1993, Perception & psychophysics.

[68]  E. Bizzi,et al.  The Cognitive Neurosciences , 1996 .

[69]  R W Cox,et al.  Language processing is strongly left lateralized in both sexes. Evidence from functional MRI. , 1999, Brain : a journal of neurology.

[70]  J. Sergent.  The cerebral balance of power: confrontation or cooperation? , 1982, Journal of experimental psychology. Human perception and performance.

[71]  R. Ivry,et al.  The two sides of perception , 1997 .

[72]  R. S. J. Frackowiak,et al.  Hemispheric specialization for global and local processing: the effect of stimulus category , 1997, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[73]  S. Hevenor,et al.  The effect of variability of unattended information on global and local processing: evidence for lateralization at early stages of processing , 2000, Neuropsychologia.

[74]  Scott O. Murray,et al.  Hemispheric Asymmetry in Global/Local Processing: Effects of Stimulus Position and Spatial Frequency , 2002, NeuroImage.

[75]  F. Kitterle,et al.  Hemispheric asymmetry in the processing of absolute versus relative spatial frequency , 1991, Brain and Cognition.

[76]  Nathalie Guyader,et al.  Image phase or amplitude? Rapid scene categorization is an amplitude-based process. , 2004, Comptes rendus biologies.